A systematic review of the safety of probiotics

Didari, Tina; Solki, Sara; Mozaffari, Shilan; Nikfar, Shekoufeh; Abdollahi, Mohammad

doi:10.1517/14740338.2014.872627

Cited by 367Probiotics and Fermented FoodsGut microbiota and healthComplementary and Alternative Medicine Studies

A systematic review of the safety of probiotics

Didari, Tina, Solki, Sara, Mozaffari, Shilan, Nikfar, Shekoufeh, Abdollahi, Mohammad·2014·Expert Opinion on Drug Safety

DOI 10.1517/14740338.2014.872627

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Abstract

INTRODUCTION: There is growing evidence on the use of probiotics in various diseases, especially in gastrointestinal (GI) diseases. Although probiotics have been found helpful in many illnesses, they do not always seem to be safe. Through interference with commensal microflora, they can result in opportunistic performances in the host due to bacterimia and fungemia. Since considerable numbers of consumers use probiotic products worldwide, assurance of safety of these products is necessary. AREAS COVERED: This review evaluates all the existing information about the safety of probiotics in humans and animal models up to May 2013. In all eligible published studies in which adverse effects and tolerability of probiotics were investigated and reported, no language limitations were applied. The main key search terms were 'probiotics,' 'safety,' 'side effects,' 'clinical trial' and 'adverse effects.' The vast majority of trials investigated Bifidobacterium (B) and Lactobacillus (L) species. EXPERT OPINION: The main observed adverse effects of probiotics were sepsis, fungemia and GI ischemia. Generally, critically ill patients in intensive care units, critically sick infants, postoperative and hospitalized patients and patients with immune-compromised complexity were the most at-risk populations. While the overwhelming existing evidence suggests that probiotics are safe, complete consideration of risk-benefit ratio before prescribing is recommended.

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A systematic literature review of probiotic safety published in 2014 reported that the overwhelming existing evidence suggests that probiotics are safe for the general population, and that critically ill patients, postoperative and hospitalized patients and immunocompromised patients were the most at-risk groups wherein adverse events occurred.
“A systematic literature review of probiotic safety published in 2014 reported that “the overwhelming existing evidence suggests that probiotics are safe” for the general population, and that critically ill patients, postoperative and hospitalized patients and immunocompromised patients were the most at-risk groups wherein AEs occurred [220].”
From International Society of Sports Nutrition Position Stand: Probiotics (2019) · cites this paper as [220]

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The pros, cons, and many unknowns of probiotics
Suez, J., Zmora, N., Segal, E., & Elinav, E. (2019) · Nature Medicine · doi:10.1038/s41591-019-0439-x · Cited by 1,398 · see citing works
Mechanisms of action of probiotics
Plaza-Diaz, J., Ruiz-Ojeda, F. J., Gil-Campos, M., & Gil, A. (2019) · Advances in Nutrition · doi:10.1093/advances/nmy063 · Cited by 1,423 · see citing works
“The effects of probiotics on host health have been reported in many articles, reviews, and systematic reviews (12, 13).”
Background
Microorganisms with Claimed Probiotic Properties: An Overview of Recent Literature
Fijan, S. (2014) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph110504745 · Cited by 1,059 · see citing works
“The most common types of microorganisms used as probiotics are lactic acid bacteria and bifidobacteria, although other bacteria and certain yeasts are also used [17].”
Background
Probiotics for the prevention of pediatric antibiotic-associated diarrhea
Goldenberg, J. Z., Lytvyn, L., Steurich, J., Parkin, P. C., Mahant, S., & Johnston, B. C. (2015) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd004827.pub4 · Cited by 625 · see citing works
The gut microbiota influences anticancer immunosurveillance and general health
Routy, B., Gopalakrishnan, V., Daillère, R., Zitvogel, L., Wargo, J. A., & Kroemer, G. (2018) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-018-0006-2 · Cited by 523 · see citing works
Prebiotics and Probiotics in Digestive Health
Quigley, E. M. M. (2018) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2018.09.028 · Cited by 387 · see citing works
The Unregulated Probiotic Market
de Simone, C. (2019) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2018.01.018 · Cited by 317 · see citing works
Effectiveness of probiotics in irritable bowel syndrome: Updated systematic review with meta-analysis
Didari, T. (2015) · World Journal of Gastroenterology · doi:10.3748/wjg.v21.i10.3072 · Cited by 356 · see citing works
Self-citation
International Society of Sports Nutrition Position Stand: Probiotics
Jäger, R., Mohr, A. E., Carpenter, K. C., Kerksick, C. M., Purpura, M., Moussa, A., Townsend, J. R., Lamprecht, M., West, N. P., Black, K., et al. (2019) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-019-0329-0 · Cited by 277 · see citing works
Probiotics for the prevention of pediatric antibiotic-associated diarrhea
Guo, Q., Goldenberg, J. Z., Humphrey, C., El Dib, R., & Johnston, B. C. (2019) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd004827.pub5 · Cited by 275 · see citing works
Probiotics, Prebiotics, Synbiotics, Postbiotics, and Obesity: Current Evidence, Controversies, and Perspectives
Vallianou, N. G., Stratigou, T., Christodoulatos, G. S., Tsigalou, C., & Dalamaga, Μ. (2020) · Current Obesity Reports · doi:10.1007/s13679-020-00379-w · Cited by 251 · see citing works
Microbiota Supplementation with Bifidobacterium and Lactobacillus Modifies the Preterm Infant Gut Microbiota and Metabolome: An Observational Study
Alcon-Giner, C., Dalby, M. J., Caim, S., Ketskemety, J., Shaw, A., Sim, K., Lawson, M. A., Kiu, R., Leclaire, C., Chalklen, L., et al. (2020) · Cell Reports Medicine · doi:10.1016/j.xcrm.2020.100077 · Cited by 229 · see citing works
“Concerns have been raised about the safety of using probiotic bacteria in vulnerable individuals.(55) However, no adverse effects were observed to result from over 5 years of routine clinical use of probiotics used in this study.”
Background
Gut Microbiota and Gestational Diabetes Mellitus: A Review of Host-Gut Microbiota Interactions and Their Therapeutic Potential
Hasain, Z., Mokhtar, N. M., Kamaruddin, N. A., Ismail, N. A. M., Razalli, N. H., Gnanou, J. V., & Ali, R. A. R. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00188 · Cited by 234 · see citing works
“Consumption of probiotics requires constant monitoring, as some adverse effects, such as systemic infections, mild gastrointestinal upset, and skin complications, have been reported in ill infants, elderly, immunocompromised individuals, and hospitalized patients (Didari et al., 2014; Sotoudegan et al., 2019).”
Background
Probiotic improves symptomatic and viral clearance in Covid19 outpatients: a randomized, quadruple-blinded, placebo-controlled trial
Gutiérrez‐Castrellón, P., Gandara-Martí, T., y Abreu, A. T. A., Nieto-Rufino, C. D., López-Orduña, E., Jiménez–Escobar, I., Jiménez-Gutiérrez, C., López‐Velázquez, G., & Espadaler, J. (2022) · Gut Microbes · doi:10.1080/19490976.2021.2018899 · Cited by 216 · see citing works
Antidepressive Mechanisms of Probiotics and Their Therapeutic Potential
Yong, S. J., Tong, T., Chew, J., & Lim, W. L. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01361 · Cited by 217 · see citing works
Diet Supplementation, Probiotics, and Nutraceuticals in SARS-CoV-2 Infection: A Scoping Review
Infusino, F., Marazzato, M., Mancone, M., Fedele, F., Mastroianni, C. M., Severino, P., Ceccarelli, G., Santinelli, L., Cavarretta, E., Marullo, A. G. M., et al. (2020) · Nutrients · doi:10.3390/nu12061718 · Cited by 202 · see citing works
“Similarly, in patients with severe disease and in critically ill patients, probiotic administration needs to be cautiously evaluated, and important safety concerns need to be considered when administering bacterial supplements [89].”
Background
Lipid-modifying effects of nutraceuticals: An evidence-based approach
Sahebkar, A., Șerban, M.-C., Gluba-Brzózka, A., Mikhailidis, D. P., Cicero, A. F. G., Rysz, J., & Banach, M. (2016) · Nutrition · doi:10.1016/j.nut.2016.04.007 · Cited by 188 · see citing works
The beneficial effects of Lactobacillus reuteri ADR-1 or ADR-3 consumption on type 2 diabetes mellitus: a randomized, double-blinded, placebo-controlled trial
Hsieh, M., Tsai, W.-H., Jheng, Y.-P., Su, S., Wang, S., Lin, C., Chen, Y.-H., & Chang, W. (2018) · Scientific Reports · doi:10.1038/s41598-018-35014-1 · Cited by 182 · see citing works
The involvement of gut microbiota in inflammatory bowel disease pathogenesis: Potential for therapy
Cammarota, G., Ianiro, G., Cianci, R., Bibbò, S., Gasbarrini, A., & Currò, D. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.12.006 · Cited by 180 · see citing works
“available systematic reviews of the literature agree on the partial, but not total, safety of probiotics (Didari et al., 2014; Whelan & Myers, 2010).”
Background
Effects of probiotic supplements on insulin resistance in gestational diabetes mellitus: A double‐blind randomized controlled trial
Kijmanawat, A., Panburana, P., Reutrakul, S., & Tangshewinsirikul, C. (2018) · Journal of Diabetes Investigation · doi:10.1111/jdi.12863 · Cited by 176 · see citing works
A critical review of antibiotic resistance in probiotic bacteria
Li, T., Teng, D., Mao, R., Hao, Y., Wang, X., & Wang, J. (2020) · Food Research International · doi:10.1016/j.foodres.2020.109571 · Cited by 172 · see citing works
Probiotics interaction with foodborne pathogens: a potential alternative to antibiotics and future challenges
Wan, M. L. Y., Forsythe, S. J., & El-Nezami, H. S. (2018) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2018.1490885 · Cited by 180 · see citing works
“…and Bifidobacterium species are commonly used as probiotics in fermented dairy products (Kirpich and McClain 2012), although other bacteria including Enterococcus spp., Leuconostoc spp. and certain yeasts such as Saccharomyces spp. have also been used as probiotics (Didari et al. 2014).”
Method
Probiotics, fibre and herbal medicinal products for functional and inflammatory bowel disorders
Currò, D., Ianiro, G., Pecere, S., Bibbò, S., & Cammarota, G. (2017) · British Journal of Pharmacology · doi:10.1111/bph.13632 · Cited by 160 · see citing works
“Some systematic reviews of the literature have tried to address it and they agreed that probiotics can be considered partially, but not totally, safe (Whelan and Myers, 2010; Didari et al., 2014).”
Background
Brain fogginess, gas and bloating: a link between SIBO, probiotics and metabolic acidosis
Rao, S. S. C., Rehman, A., Yu, S. W. B., & de Andino, N. M. (2018) · Clinical and Translational Gastroenterology · doi:10.1038/s41424-018-0030-7 · Cited by 163 · see citing works
Harms Reporting in Randomized Controlled Trials of Interventions Aimed at Modifying Microbiota: A Systematic Review
Bafeta, A., Koh, M., Riveros, C., & Ravaud, P. (2018) · Annals of Internal Medicine · doi:10.7326/m18-0343 · Cited by 162 · see citing works
“Median patients randomly assigned per study (interquartile range), n 62 (43-120)”
Pregnancy outcomes in women taking probiotics or prebiotics: a systematic review and meta-analysis
Jarde, A., Lewis-Mikhael, A.-M., Moayyedi, P., Stearns, J. C., Collins, S. M., Beyene, J., & McDonald, S. D. (2018) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-017-1629-5 · Cited by 161 · see citing works
“They can be given as biological supplements or in food [3] such as yogurt, [4] making them readily available for consumption.”
Background
Encapsulation: A Strategy to Deliver Therapeutics and Bioactive Compounds?
Klojdová, I., Milota, T., Smetanová, J., & Stathopoulos, C. E. (2023) · Pharmaceuticals · doi:10.3390/ph16030362 · Cited by 155 · see citing works
“The use of probiotics has been associated with a higher risk of infection and/or morbidity in young infants and postoperative, hospitalized or immuno-compromised patients, in part due to bacteraemia and fungaemia [54].”
Background
Lactic acid bacteria: reviewing the potential of a promising delivery live vector for biomedical purposes
Cano‐Garrido, O., Seras‐Franzoso, J., & García‐Fruitós, E. (2015) · Microbial Cell Factories · doi:10.1186/s12934-015-0313-6 · Cited by 148 · see citing works
“Besides, it should be noted that some adverse effects of LAB have been reported [104] [105] [106] .”
Background
Rational use of prebiotics for gut microbiota alterations: Specific bacterial phylotypes and related mechanisms
Wang, S., Xiao, Y., Tian, F., Zhao, J., Zhang, H., Zhai, Q., & Chen, W. (2020) · Journal of Functional Foods · doi:10.1016/j.jff.2020.103838 · Cited by 146 · see citing works
Changing our microbiome: probiotics in dermatology
Yu, Y., Dunaway, S., Champer, J., Kim, J., & Alikhan, A. (2019) · British Journal of Dermatology · doi:10.1111/bjd.18088 · Cited by 144 · see citing works
Clinical implications of preterm infant gut microbiome development
Healy, D., Ryan, C. A., Ross, R. P., Stanton, C., & Dempsey, E. M. (2021) · Nature Microbiology · doi:10.1038/s41564-021-01025-4 · Cited by 132 · see citing works
Probiotics for treating eczema
Makrgeorgou, A., Leonardi‐Bee, J., Bath-Hextall, F. J., Murrell, D. F., Tang, M. L. K., Roberts, A., & Boyle, R. J. (2018) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd006135.pub3 · Cited by 130 · see citing works
The anxiolytic effect of probiotics: A systematic review and meta-analysis of the clinical and preclinical literature
Reis, D. J., Ilardi, S. S., & Punt, S. E. W. (2018) · PLOS ONE · doi:10.1371/journal.pone.0199041 · Cited by 123 · see citing works
Crosstalk between the microbiome and cancer cells by quorum sensing peptides
Wynendaele, E., Verbeke, F., D’Hondt, M., Hendrix, A., de Wiele, C. V., Burvenich, C., Peremans, K. Y., Wever, O. D., Bracke, M., & Spiegeleer, B. M. J. D. (2015) · Peptides · doi:10.1016/j.peptides.2014.12.009 · Cited by 115 · see citing works
“bacteremia, fungemia and gastrointestinal ischemia; critically ill patients and immune-compromised individuals are the most-at-risk populations [9].”
Strategies to Improve Meat Products’ Quality
Ursachi, C. Ș., Perța-Crișan, S., & Munteanu, F. (2020) · Foods · doi:10.3390/foods9121883 · Cited by 125 · see citing works
“The main species of microorganisms used as probiotics in food products are Lactobacillus and Bifidobacterium but have also been reported a lot of other species of bacteria (Lactococcus, Enterococcus, Propionibacterium) or yeasts (Saccharomyces) that are also available [73].”
Background
Nutrition in the Intensive Care Unit—A Narrative Review
Hill, A., Elke, G., & Weimann, A. (2021) · Nutrients · doi:10.3390/nu13082851 · Cited by 114 · see citing works
“Their administration is a challenging concept with a potential impact on diarrhea and infectious complications [62,63].”
Background
Exploring biotechnological and functional characteristics of probiotic yeasts: A review
Shruthi, B., Deepa, N., Somashekaraiah, R., Adithi, G., Divyashree, S., & Sreenivasa, M. Y. (2022) · Biotechnology Reports · doi:10.1016/j.btre.2022.e00716 · Cited by 114 · see citing works
“The yeast species Debaryomyces hansenii, which have the capacity to tolerate high salt concentration, isolated from several natural environments and foods, found to obtain advantageous and useful effect for applications as probiotics in Pisces [2] .”
Background
Prebiotics and Probiotics for Gastrointestinal Disorders
Rau, S., Gregg, A., Yaceczko, S. D., & Limketkai, B. N. (2024) · Nutrients · doi:10.3390/nu16060778 · Cited by 121 · see citing works
“A 2014 systematic review described several cases of bacteremia with Lactobacillus strains ( L. rhamnosus GG, in particular) and fungemia in ICU patients with a central venous catheter receiving S. boulardii [179].”
Background
Bifidobacterium Bacteremia: Clinical Characteristics and a Genomic Approach To Assess Pathogenicity
Esaiassen, E., Hjerde, E., Cavanagh, J. P., Simonsen, G. S., & Klingenberg, C. (2017) · Journal of Clinical Microbiology · doi:10.1128/jcm.00150-17 · Cited by 108 · see citing works
“Although probiotic products generally are regarded as safe, vigilance regarding their potential virulence, antibacterial resistance, and adverse metabolic activity should be maintained, in particular, in patients with predisposing or underlying conditions, such as gastrointestinal surgery, malignancy, or immunodeficie…”
Background
Therapeutic Anti-Depressant Potential of Microbial GABA Produced by Lactobacillus rhamnosus Strains for GABAergic Signaling Restoration and Inhibition of Addiction-Induced HPA Axis Hyperactivity
Tette, F.-M., Kwofie, S. K., & Wilson, M. D. (2022) · Current Issues in Molecular Biology · doi:10.3390/cimb44040096 · Cited by 114 · see citing works
Role of probiotics in stimulating the immune system in viral respiratory tract infections: A narrative review
Lehtoranta, L., Latvala, S., & Lehtinen, M. J. (2020) · Nutrients · doi:10.3390/nu12103163 · Cited by 103 · see citing works
Using probiotics for type 2 diabetes mellitus intervention: Advances, questions, and potential
Sun, Z., Sun, X., Li, J., Li, Z., Hu, Q., Li, L., Hao, X., Song, M., & Li, C. (2020) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2018.1547268 · Cited by 117 · see citing works
“Although probiotic are generally regarded as safe (GRAS), careful consideration of side effects before application is still recommended, as adverse effects of probiotics, like sepsis, fungemia, and gastrointestinal ischemia are occasionally reported, especially in critically ill patients (Didari et al. 2014).”
Background
Shedding light on biological sex differences and microbiota–gut–brain axis: a comprehensive review of its roles in neuropsychiatric disorders
Shobeiri, P., Kalantari, A., Teixeira, A. L., & Rezaei, N. (2022) · Biology of Sex Differences · doi:10.1186/s13293-022-00422-6 · Cited by 105 · see citing works
“Probiotics including Lactobacillus and Bifidobacterium species have been evaluated as therapeutic agents in various mental and neurodegenerative disorders [332].”
Background
Functional and health-promoting properties of probiotics’ exopolysaccharides; isolation, characterization, and applications in the food industry
Pourjafar, H., Ansari, F., Sadeghi, A., Samakkhah, S. A., & Jafari, S. M. (2022) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2022.2047883 · Cited by 103 · see citing works
“Accordingly, complete consideration of risk-benefit ratio as well as in vitro, in vivo, and in situ evaluation of safety aspects before acceptance of potentially probiotic microorganisms as GRAS or qualified presumption of their safety status is recommended (Didari et al. 2014).”
Background
A practical guide for probiotics applied to the case of antibiotic-associated diarrhea in The Netherlands
Agamennone, V., Krul, C. A. M., Rijkers, G. T., & Kort, R. (2018) · BMC Gastroenterology · doi:10.1186/s12876-018-0831-x · Cited by 97 · see citing works
“patients, immuno-compromised patients are at high risk [23, 24]).”
Background
Antibiotic resistance propagation through probiotics
Daniali, M., Nikfar, S., & Abdollahi, M. (2020) · Expert Opinion on Drug Metabolism & Toxicology · doi:10.1080/17425255.2020.1825682 · Cited by 90 · see citing works
Self-citation
Recent insights into the nutritional immunomodulation of cancer‐related microRNAs
Şahin, T. Ö., Yılmaz, B., Yeşilyurt, N., Cicia, D., Szymanowska, A., Amero, P., Ağagündüz, D., & Capasso, R. (2023) · Phytotherapy Research · doi:10.1002/ptr.7937 · Cited by 87 · see citing works
“In addition, it was stated that probiotics might have side effects, as well as beneficial effects on health and safety issues, which might arise due to the use of microbial cells (Didari et al., 2014).”
Background
Probiotic – friend or foe?
Žučko, J., Starčević, A., Diminić, J., Oros, D., Mortazavian, A. M., & Putnik, P. (2020) · Current Opinion in Food Science · doi:10.1016/j.cofs.2020.01.007 · Cited by 89 · see citing works
Potential Probiotic Yeasts Sourced from Natural Environmental and Spontaneous Processed Foods
Agarbati, A., Canonico, L., Marini, E., Zannini, E., Ciani, M., & Comitini, F. (2020) · Foods · doi:10.3390/foods9030287 · Cited by 85 · see citing works
“Currently, it represents the most common human probiotic yeast studied in detail and available on the market [13].”
Background
Comparative effectiveness of probiotic strains for the treatment of pediatric atopic dermatitis: A systematic review and network meta‐analysis
Tan‐Lim, C. S. C., Esteban‐Ipac, N. A. R., Mantaring, J. B. V., Shih‐Yen, E. C., Recto, M. S. T., Sison, O. T., & Alejandria, M. M. (2020) · Pediatric Allergy and Immunology · doi:10.1111/pai.13305 · Cited by 84 · see citing works
Effect of Bifidobacterium on osteoclasts: TNF-α/NF-κB inflammatory signal pathway-mediated mechanism
Wu, Y., Yang, Y., Wang, L., Chen, Y., Han, X., Sun, L., Chen, H., & Chen, Q. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1109296 · Cited by 83 · see citing works
“Several research and clinical studies have demonstrated that, probiotics, despite their disease-prevention and treatment effects, are not absolutely safe or without side effects (33).”
Background
Probiotics: Should All Patients Take Them?
Katkowska, M., Garbacz, K., & Kusiak, A. (2021) · Microorganisms · doi:10.3390/microorganisms9122620 · Cited by 82 · see citing works
“Furthermore, it has been shown that, although very rarely, probiotic strains cause infections in humans [26,28,29].”
Background
Gut microbiota and sepsis: from pathogenesis to novel treatments
Kullberg, R. F. J., Wiersinga, W. J., & Haak, B. W. (2021) · Current Opinion in Gastroenterology · doi:10.1097/mog.0000000000000781 · Cited by 78 · see citing works
“difficile infection have been earlier described, especially in critically ill patients and infants [39,40].”
Background
Harms Reporting in Randomized Controlled Trials of Interventions Aimed at Modifying Microbiota
Bafeta, A., Koh, M., Riveros, C., & Ravaud, P. (2019) · Annals of Internal Medicine · doi:10.7326/l18-0562 · Cited by 76 · see citing works
Diversity of the bacteriocins, their classification and potential applications in combat of antibiotic resistant and clinically relevant pathogens
Choi, G. H., Holzapfel, W. H., & Todorov, S. D. (2022) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2022.2090227 · Cited by 78 · see citing works
“In addition to the LAB, other Gram-positive bacteria such as the bifidobacteria belonging to the phylum Actinobacteria, along with certain Gram-negative bacteria belonging to the Proteobacteria have been applied as probiotics (Didari et al. 2014).”
Background
Randomized controlled trial demonstrates response to a probiotic intervention for metabolic syndrome that may correspond to diet
Wastyk, H. C., Perelman, D., Topf, M. A., Fragiadakis, G. K., Robinson, J. L., Sonnenburg, J. L., Gardner, C. D., & Sonnenburg, E. D. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2178794 · Cited by 68 · see citing works
“In general, probiotic supplements are considered extremely safe, however, there have been reports that probiotics can lead to acute issues such as sepsis and gastrointestinal issues in individuals with compromised immune systems.(22) Similarly, probiotic supplementation can hinder microbiome recovery after antibiotic…”
Background
Molecular genetics for probiotic engineering: dissecting lactic acid bacteria
Suissa, R., Oved, R., Jankelowitz, G., Turjeman, S. C., Koren, O., & Kolodkin‐Gal, I. (2021) · Trends in Microbiology · doi:10.1016/j.tim.2021.07.007 · Cited by 68 · see citing works
Mucosal adhesion and anti-inflammatory effects of Lactobacillus rhamnosus GG in the human colonic mucosa: A proof-of-concept study
Pagnini, C., Corleto, V. D., Martorelli, M., Lanini, C., D’Ambra, G., Giulio, E. D., & Fave, G. D. (2018) · World Journal of Gastroenterology · doi:10.3748/wjg.v24.i41.4652 · Cited by 67 · see citing works
Approach to the diagnosis and management of dysbiosis
Alagiakrishnan, K., Morgadinho, J., & Halverson, T. (2024) · Frontiers in Nutrition · doi:10.3389/fnut.2024.1330903 · Cited by 75 · see citing works
“In immunocompromised or critically ill people, probiotics can increase opportunistic infections and so a risk benefit assessment should be done before recommending these products (235).”
Background
High resolution melting analysis (HRM) as a new tool for the identification of species belonging to the Lactobacillus casei group and comparison with species-specific PCRs and multiplex PCR
Iacumin, L., Ginaldi, F., Manzano, M., Anastasi, V., Reale, A., Zotta, T., Rossi, F., Coppola, R., & Comi, G. (2014) · Food Microbiology · doi:10.1016/j.fm.2014.08.007 · Cited by 66 · see citing works
Seven cases of Saccharomyces fungaemia related to use of probiotics
Roy, U., Jessani, L. G., Rudramurthy, S. M., Gopalakrishnan, R., Dutta, S., Chakravarty, C., Jillwin, J., & Chakrabarti, A. (2017) · Mycoses · doi:10.1111/myc.12604 · Cited by 66 · see citing works
Comparative effectiveness of probiotic strains on the prevention of pediatric atopic dermatitis: A systematic review and network meta-analysis
Tan‐Lim, C. S. C., Esteban‐Ipac, N. A. R., Recto, M. S. T., Castor, M. A. R., Casis‐Hao, R. J., & Nano, A. L. M. (2021) · Pediatric Allergy and Immunology · doi:10.1111/pai.13514 · Cited by 65 · see citing works
The Effect of Bifidobacterium animalis ssp. lactis HN019 on Cellular Immune Function in Healthy Elderly Subjects: Systematic Review and Meta-Analysis
Miller, L. E., Lehtoranta, L., & Lehtinen, M. J. (2017) · Nutrients · doi:10.3390/nu9030191 · Cited by 64 · see citing works
“lactis HN019 has an impact on immune cell function in blood; however, it remains unknown if the stimulatory effect would have been maintained in longer term consumption [45].”
Background
In vitro investigation of Debaryomyces hansenii strains for potential probiotic properties
Ochangco, H. S., Gamero, A., Smith, I. M., Christensen, J. E., Jespersen, L., & Arneborg, N. (2016) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-016-2109-1 · Cited by 59 · see citing works
Contemporary meta-analysis of short-term Probiotic consumption on gastrointestinal transit
Miller, L. E., Zimmermann, A. K., & Ouwehand, A. C. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i21.5122 · Cited by 57 · see citing works
Probiotics for oral and vulvovaginal candidiasis: A review
Shenoy, A., & Gottlieb, A. B. (2019) · Dermatologic Therapy · doi:10.1111/dth.12970 · Cited by 78 · see citing works
Probiotics and their Beneficial Health Effects
Zaib, S., Hayat, A., & Khan, I. A. (2023) · Mini-Reviews in Medicinal Chemistry · doi:10.2174/1389557523666230608163823 · Cited by 59 · see citing works
Effects of Probiotic Supplementation during Pregnancy on the Future Maternal Risk of Metabolic Syndrome
Obuchowska, A., Gorczyca, K., Standyło, A., Obuchowska, K., Kimber-Trojnar, Ż., Wierzchowska-Opoka, M., & Leszczyńska‐Gorzelak, B. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158253 · Cited by 56 · see citing works
“Nevertheless, side effects such as systemic infections, mild gastrointestinal disturbances and skin complications have been reported [5,10].”
Background
A cell-free, biomimetic hydrogel based on probiotic membrane vesicles ameliorates wound healing
Kuhn, T., Aljohmani, A., Frank, N. A., Zielke, L., Mehanny, M., Laschke, M. W., Koch, M., Hoppstädter, J., Kiemer, A. K., Yildiz, D., et al. (2023) · Journal of Controlled Release · doi:10.1016/j.jconrel.2023.12.011 · Cited by 56 · see citing works
Immunosuppression and probiotics: are they effective and safe?
Stadlbauer, V. (2015) · Beneficial Microbes · doi:10.3920/bm2015.0065 · Cited by 56 · see citing works
Invasive Infections Associated with the Use of Probiotics in Children: A Systematic Review
D’Agostin, M., Squillaci, D., Lazzerini, M., Barbi, E., Wijers, L., & Lozzo, P. D. (2021) · Children · doi:10.3390/children8100924 · Cited by 56 · see citing works
“However, only a few systematic safety studies have been carried out, particularly in vulnerable populations, and most of the existing published studies on probiotics have not specifically reported safety, leaving uncertainties regarding their potential risks [15,16].”
Background
Probiotics and Their Effect on Surgical Wound Healing: A Systematic Review and New Insights into the Role of Nanotechnology
Bekiaridou, Α., Karlafti, E., Oikonomou, I. M., Ioannidis, A., & Papavramidis, T. S. (2021) · Nutrients · doi:10.3390/nu13124265 · Cited by 55 · see citing works
“Theoretical risks that include systemic infections and excessive immune response have been described without observational data [45,46].”
Background
Probiotics and postbiotics play a role in maintaining dermal health
Rawal, S., & Ali, S. A. (2023) · Food & Function · doi:10.1039/d3fo00152k · Cited by 56 · see citing works
The potential role of prebiotics, probiotics, and synbiotics in adjuvant cancer therapy especially colorectal cancer
Alam, Z., Shang, X., Effat, K., Kanwal, F., He, X., Li, Y., Xu, C., Niu, W., War, A. R., & Zhang, Y. (2022) · Journal of Food Biochemistry · doi:10.1111/jfbc.14302 · Cited by 53 · see citing works
Natural nutraceuticals, especially functional foods, their major bioactive components, formulation, and health benefits for disease prevention: an overview
Awuchi, C. G., & Okpala, C. O. R. (2022) · Journal of Food Bioactives · doi:10.31665/jfb.2022.18317 · Cited by 52 · see citing works
Value of Probiotics in Canine and Feline Gastroenterology
Schmitz, S. S. (2020) · Veterinary Clinics of North America Small Animal Practice · doi:10.1016/j.cvsm.2020.09.011 · Cited by 52 · see citing works
Lactobacillus rhamnosus GG alleviates radiation-induced intestinal injury by modulating intestinal immunity and remodeling gut microbiota
Zhang, L., Xu, J.-Y., Xing, Y., Wu, P., Jin, Y.-W., Wei, W., Zhao, L., Yang, J., Chen, G., & Qin, L. (2024) · Microbiological Research · doi:10.1016/j.micres.2024.127821 · Cited by 50 · see citing works
Probiotics and synbiotics for preventing postoperative infectious complications in colorectal cancer patients: a systematic review and meta-analysis
Chen, Y., Qi, A., Teng, D., Li, S., Yan, Y., Hu, S., & Du, X. (2022) · Techniques in Coloproctology · doi:10.1007/s10151-022-02585-1 · Cited by 49 · see citing works
“Therefore, probiotics and synbiotics should be used in consideration of their possible side effects, which need to be confirmed by more studies [38].”
Background
Nutraceuticals as modulators of gut microbiota: Role in therapy
Quigley, E. M. M. (2019) · British Journal of Pharmacology · doi:10.1111/bph.14902 · Cited by 47 · see citing works
Probiotics in obstetrics and gynaecology
Griffin, C. J. (2015) · Australian and New Zealand Journal of Obstetrics and Gynaecology · doi:10.1111/ajo.12303 · Cited by 47 · see citing works
Saccharomyces cerevisiae fungemia after probiotic treatment in an intensive care unit patient
Kara, İ., Yıldırım, F., ., O. O., Erganiş, S., Aydoğdu, M., Dizbay, M., Gürsel, G., & Kalkancı, A. (2017) · Journal de Mycologie Médicale · doi:10.1016/j.mycmed.2017.09.003 · Cited by 46 · see citing works
A comprehensive review of probiotic claims regulations: Updates from Asia-Pacific, United States, and Europe
Garg, V., Velumani, D., Lin, Y.-C., & Haye, A. (2024) · PharmaNutrition · doi:10.1016/j.phanu.2024.100423 · Cited by 44 · see citing works
A Brief Overview on Probiotics: The Health Friendly Microbes
Mishra, S., & Acharya, S. (2021) · Biomedical & Pharmacology Journal · doi:10.13005/bpj/2285 · Cited by 46 · see citing works
Probiotics and their applications in functional foods: a health perspective
Amin, M. R., Biswas, A. P., Tasnim, M., Islam, M. N., & Azam, M. S. (2025) · Applied Food Research · doi:10.1016/j.afres.2025.101193 · Cited by 46 · see citing works
Gut Microbiome and Common Variable Immunodeficiency: Few Certainties and Many Outstanding Questions
Varricchi, G., Poto, R., Ianiro, G., Punziano, A., Marone, G., Gasbarrini, A., & Spadaro, G. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.712915 · Cited by 44 · see citing works
“Finally, synbiotics themselves can be associated with adverse events and their safety profile is often overlooked (205, 206).”
Background
Dealing with the remaining controversies of probiotic safety
van den Nieuwboer, M., & Claassen, E. (2019) · Beneficial Microbes · doi:10.3920/bm2018.0159 · Cited by 41 · see citing works
Probiotic-Associated Aspiration Pneumonia Due to Lactobacillus rhamnosus
Doern, C. D., Nguyen, S. T., Afolabi, F., & Burnham, C.-A. D. (2014) · Journal of Clinical Microbiology · doi:10.1128/jcm.01065-14 · Cited by 41 · see citing works
“Lactobacilli are low-virulence organisms that are commensals of the genitourinary and gastrointestinal tracts and are commonly used as probiotic supplements (15).”
Background
Antibiotics and probiotics in inflammatory bowel disease: when to use them?
Abraham, B. P., & Quigley, E. M. M. (2019) · Frontline Gastroenterology · doi:10.1136/flgastro-2018-101057 · Cited by 39 · see citing works
“62 63 Since probiotic strains typically do not colonise the adult colon and repeated or indefinite use is required for an ongoing effect, long-term maintenance studies in IBD are needed.”
The potential role of interventions impacting on gut-microbiota in epilepsy
Iannone, L. F., Gómez-Eguílaz, M., Citaro, R., & Russo, E. (2020) · Expert Review of Clinical Pharmacology · doi:10.1080/17512433.2020.1759414 · Cited by 38 · see citing works
Probiotics and human lactational mastitis: A scoping review
Barker, M., Adelson, P., Peters, M. D. J., & Steen, M. (2020) · Women and Birth · doi:10.1016/j.wombi.2020.01.001 · Cited by 36 · see citing works
Gut Microbiota Modulation: Implications for Infection Control and Antimicrobial Stewardship
Tan, G. S. E., Tay, H. L., Tan, S. H., Lee, T. H., Ng, T. M., & Lye, D. C. (2020) · Advances in Therapy · doi:10.1007/s12325-020-01458-z · Cited by 37 · see citing works
Altered gut microbiome associated with overactive bladder and daily urinary urgency
Okamoto, T., Hatakeyama, S., Imai, A., Yamamoto, H., Yoneyama, T., Mori, K., Yoneyama, T., Hashimoto, Y., Nakaji, S., & Οhyama, C. (2020) · World Journal of Urology · doi:10.1007/s00345-020-03243-7 · Cited by 34 · see citing works
“Some bacteria of the genus Bifidobacterium may play critical beneficial roles and have been used as probiotics [28, 29].”
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Probiotics in health and disease: fooling Mother Nature?
Abid, M. B., & Koh, C. J. (2019) · Infection · doi:10.1007/s15010-019-01351-0 · Cited by 35 · see citing works
Strategies for the eradication of extended-spectrum beta-lactamase or carbapenemase-producing Enterobacteriaceae intestinal carriage
Catho, G., & Huttner, B. D. (2019) · Expert Review of Anti-infective Therapy · doi:10.1080/14787210.2019.1645007 · Cited by 33 · see citing works
“So far there is no evidence for the impact of probiotics on decolonization and caution should be taken before applying probiotics for this purpose in routine clinical practice, since manipulation of the microbiome could lead to unintended consequences and probiotics may also be the cause of infections, particularly in…”
Background
Strategies for the Development of Bioprotective Cultures in Food Preservation
Souza, L. V., Martins, E., Moreira, I. M. F. B., & de Carvalho, A. F. (2022) · International Journal of Microbiology · doi:10.1155/2022/6264170 · Cited by 32 · see citing works
Nutritional and metabolic modulation of inflammation in critically ill patients: a narrative review of rationale, evidence and grey areas
Rousseau, A., & Martindale, R. G. (2024) · Annals of Intensive Care · doi:10.1186/s13613-024-01350-x · Cited by 32 · see citing works
“Due to their immunocompromised status, critically ill patients are at risk of bacteremia or fungemia secondary to probiotics administration [113].”
Background
Effects of probiotics on blood glucose, biomarkers of inflammation and oxidative stress in pregnant women with gestational diabetes mellitus: A meta-analysis of randomized controlled trials
Chen, Y., Yue, R., Zhang, B., Li, Z., Shui, J., & Huang, X. (2019) · Medicina Clínica · doi:10.1016/j.medcli.2019.05.041 · Cited by 32 · see citing works
A novel probiotic strain of Lactobacillus fermentum TIU19 isolated from Haria beer showing both in vitro antibacterial and antibiofilm properties upon two multi resistant uro-pathogen strains
Das, S., Vishakha, K., Banerjee, S., Bera, T., Mondal, S., & Ganguli, A. (2022) · Current Research in Microbial Sciences · doi:10.1016/j.crmicr.2022.100150 · Cited by 32 · see citing works
Safety of Probiotic Bacteria
Abdollahi, M. R., Abdolghaffari, A. H., Gooshe, M., & Ghasemi‐Niri, S. F. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-802189-7.00015-0 · Cited by 32 · see citing works
Self-citation
Postbiotic lactobacilli induce cutaneous antimicrobial response and restore the barrier to inhibit the intracellular invasion of Staphylococcus aureus in vitro and ex vivo
Dinić, M., Burgess, J. L., Lukić, J., Catanuto, P., Radojević, D., Marjanović, J., Verpile, R., Thaller, S. R., Gonzalez, T., Golić, N., et al. (2024) · The FASEB Journal · doi:10.1096/fj.202400054rr · Cited by 31 · see citing works
“9,10 Commercially available probiotics can have a different ratio of living and dead bacterial cells, depending on the methods of formulation, which can affect biological effect after application.”

Authors: Didari, T., Solki, S., Mozaffari, S., Nikfar, S., & Abdollahi, M.
Affiliations: Islamic Azad University, Tehran (IR)
Pharmaceutical Sciences Research Center (IR)
Ministry of Health and Medical Education (IR)
ORCID: Didari, Tina
Mozaffari, Shilan
Nikfar, Shekoufeh
Abdollahi, Mohammad
Venue: Expert Opinion on Drug Safety
Publisher: Informa Healthcare
Published: 2014-01-03
Volume: 13
Issue: 2
Pages: 227-239
ISSN: 1474-0338 (ISSN-L)
1744-764X
DOI: 10.1517/14740338.2014.872627
OpenAlex: W2125631968
Cited by: 367
References: 117
Citations by year: 2026: 27 · 2025: 44 · 2024: 32 · 2023: 42 · 2022: 41 · 2021: 41 · 2020: 38 · 2019: 28 · 2018: 27 · 2017: 14 · 2016: 11 · 2015: 14 · 2014: 8
FWCI: 1.94
Type: journal article
Language: en
Open access: closed
Locations: Expert Opinion on Drug Safety (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Medicine › Complementary and alternative medicine › Complementary and Alternative Medicine Studies
Keywords: probiotics, probiotic safety, adverse effects, sepsis, fungemia, gastrointestinal ischemia, Bifidobacterium, Lactobacillus, opportunistic infections, commensal microbiota, critically ill patients, immunocompromised patients, risk-benefit ratio
MeSH terms: Animals, Bifidobacterium, Humans, Lactobacillus, Safety, Probiotics, Drug-Related Side Effects and Adverse Reactions

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A systematic review of the safety of probiotics

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